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Title: Structural basis for preferential binding of human TCF4 to DNA containing 5-carboxylcytosine

Authors:
 [1];  [1];  [2]; ORCiD logo [2];  [1];  [3]; ORCiD logo [1]
  1. Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA
  2. Center for Epigenetics & Disease Prevention, Institute of Biosciences and Technology, Texas A&M University, Houston, TX 77030, USA
  3. Department of Medical Microbiology and Immunology, and Program in Bioinformatics, The University of Toledo College of Medicine and Life Sciences, Toledo, OH 43614, USA
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
National Institutes of Health (NIH)
OSTI Identifier:
1577156
Resource Type:
Journal Article
Journal Name:
Nucleic Acids Research
Additional Journal Information:
Journal Volume: 47; Journal Issue: (16) ; 09, 2019; Journal ID: ISSN 0305-1048
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
ENGLISH

Citation Formats

Yang, Jie, Horton, John R., Li, Jia, Huang, Yun, Zhang, Xing, Blumenthal, Robert M., and Cheng, Xiaodong. Structural basis for preferential binding of human TCF4 to DNA containing 5-carboxylcytosine. United States: N. p., 2019. Web. doi:10.1093/nar/gkz381.
Yang, Jie, Horton, John R., Li, Jia, Huang, Yun, Zhang, Xing, Blumenthal, Robert M., & Cheng, Xiaodong. Structural basis for preferential binding of human TCF4 to DNA containing 5-carboxylcytosine. United States. doi:10.1093/nar/gkz381.
Yang, Jie, Horton, John R., Li, Jia, Huang, Yun, Zhang, Xing, Blumenthal, Robert M., and Cheng, Xiaodong. Mon . "Structural basis for preferential binding of human TCF4 to DNA containing 5-carboxylcytosine". United States. doi:10.1093/nar/gkz381.
@article{osti_1577156,
title = {Structural basis for preferential binding of human TCF4 to DNA containing 5-carboxylcytosine},
author = {Yang, Jie and Horton, John R. and Li, Jia and Huang, Yun and Zhang, Xing and Blumenthal, Robert M. and Cheng, Xiaodong},
abstractNote = {},
doi = {10.1093/nar/gkz381},
journal = {Nucleic Acids Research},
issn = {0305-1048},
number = (16) ; 09, 2019,
volume = 47,
place = {United States},
year = {2019},
month = {5}
}

Works referenced in this record:

Transient Accumulation of 5-Carboxylcytosine Indicates Involvement of Active Demethylation in Lineage Specification of Neural Stem Cells
journal, June 2014


Model-based Analysis of ChIP-Seq (MACS)
journal, January 2008


Crystal structure of transcription factor E47: E-box recognition by a basic region helix-loop-helix dimer.
journal, April 1994

  • Ellenberger, T.; Fass, D.; Arnaud, M.
  • Genes & Development, Vol. 8, Issue 8
  • DOI: 10.1101/gad.8.8.970

Improved crystallographic models through iterated local density-guided model deformation and reciprocal-space refinement
journal, June 2012

  • Terwilliger, Thomas C.; Read, Randy J.; Adams, Paul D.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 7
  • DOI: 10.1107/S0907444912015636

Common variants conferring risk of schizophrenia
journal, July 2009

  • Stefansson, Hreinn; Ophoff, Roel A.; Steinberg, Stacy
  • Nature, Vol. 460, Issue 7256
  • DOI: 10.1038/nature08186

The Nuclear DNA Base 5-Hydroxymethylcytosine Is Present in Purkinje Neurons and the Brain
journal, April 2009


Global Epigenomic Reconfiguration During Mammalian Brain Development
journal, July 2013


Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc
journal, March 1991


Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012

  • Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel
  • Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4
  • DOI: 10.1107/S0907444912001308

The Phyre2 web portal for protein modeling, prediction and analysis
journal, May 2015

  • Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M.
  • Nature Protocols, Vol. 10, Issue 6
  • DOI: 10.1038/nprot.2015.053

Lmx1a drives Cux2 expression in the cortical hem through activation of a conserved intronic enhancer
journal, February 2019

  • Fregoso, Santiago P.; Dwyer, Brett E.; Franco, Santos J.
  • Development, Vol. 146, Issue 5
  • DOI: 10.1242/dev.170068

Functional analysis of TCF4 missense mutations that cause Pitt-Hopkins syndrome
journal, July 2012

  • Forrest, Marc; Chapman, Ria M.; Doyle, A. Michelle
  • Human Mutation, Vol. 33, Issue 12
  • DOI: 10.1002/humu.22160

Introducing Pitt-Hopkins syndrome-associated mutations of TCF4 to Drosophila daughterless
journal, November 2015

  • Tamberg, L.; Sepp, M.; Timmusk, T.
  • Biology Open, Vol. 4, Issue 12
  • DOI: 10.1242/bio.014696

The Psychiatric Risk Gene Transcription Factor 4 (TCF4) Regulates Neurodevelopmental Pathways Associated With Schizophrenia, Autism, and Intellectual Disability
journal, December 2017

  • Forrest, Marc P.; Hill, Matthew J.; Kavanagh, David H.
  • Schizophrenia Bulletin, Vol. 44, Issue 5
  • DOI: 10.1093/schbul/sbx164

MAX is an epigenetic sensor of 5-carboxylcytosine and is altered in multiple myeloma
journal, November 2016

  • Wang, Dongxue; Hashimoto, Hideharu; Zhang, Xing
  • Nucleic Acids Research, Vol. 45, Issue 5
  • DOI: 10.1093/nar/gkw1184

Association of Myn, the murine homolog of Max, with c-Myc stimulates methylation-sensitive DNA binding and ras cotransformation
journal, May 1991


Genome-wide Analysis Reveals TET- and TDG-Dependent 5-Methylcytosine Oxidation Dynamics
journal, April 2013


Helix-Loop-Helix Proteins: Regulators of Transcription in Eucaryotic Organisms
journal, January 2000


Genome-wide Profiling of 5-Formylcytosine Reveals Its Roles in Epigenetic Priming
journal, April 2013


Crystal Structure of a Complex of DNA with One AT-Hook of HMGA1
journal, May 2012


The emerging roles of TCF4 in disease and development
journal, June 2014


Tcf4 Regulates Synaptic Plasticity, DNA Methylation, and Memory Function
journal, September 2016


Detecting and interpreting DNA methylation marks
journal, December 2018


Mutational, functional, and expression studies of the TCF4 gene in Pitt-Hopkins syndrome
journal, April 2009

  • de Pontual, Lo��c; Mathieu, Yves; Golzio, Christelle
  • Human Mutation, Vol. 30, Issue 4
  • DOI: 10.1002/humu.20935

Carboxylation of cytosine (5caC) in the CG dinucleotide in the E-box motif (CGCAG|GTG) increases binding of the Tcf3|Ascl1 helix-loop-helix heterodimer 10-fold
journal, June 2014

  • Golla, Jaya Prakash; Zhao, Jianfei; Mann, Ishminder K.
  • Biochemical and Biophysical Research Communications, Vol. 449, Issue 2
  • DOI: 10.1016/j.bbrc.2014.05.018

Cistrome Data Browser: expanded datasets and new tools for gene regulatory analysis
journal, November 2018

  • Zheng, Rongbin; Wan, Changxin; Mei, Shenglin
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky1094

A Druggable TCF4- and BRD4-Dependent Transcriptional Network Sustains Malignancy in Blastic Plasmacytoid Dendritic Cell Neoplasm
journal, November 2016


Tet Proteins Can Convert 5-Methylcytosine to 5-Formylcytosine and 5-Carboxylcytosine
journal, July 2011


A statistic for local intensity differences: robustness to anisotropy and pseudo-centering and utility for detecting twinning
journal, June 2003

  • Padilla, Jennifer E.; Yeates, Todd O.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 7
  • DOI: 10.1107/S0907444903007947

Simultaneous mapping of active DNA demethylation and sister chromatid exchange in single cells
journal, March 2017


Investigation of the role of TCF4 rare sequence variants in schizophrenia
journal, May 2015

  • Basmanav, F. Buket; Forstner, Andreas J.; Fier, Heide
  • American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, Vol. 168, Issue 5
  • DOI: 10.1002/ajmg.b.32318

Evidence of CNIH3 involvement in opioid dependence
journal, August 2015

  • Nelson, E. C.; Agrawal, A.; Heath, A. C.
  • Molecular Psychiatry, Vol. 21, Issue 5
  • DOI: 10.1038/mp.2015.102

Conversion of 5-Methylcytosine to 5-Hydroxymethylcytosine in Mammalian DNA by MLL Partner TET1
journal, April 2009


A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins
journal, March 1989


Crystal Structure of E47−NeuroD1/Beta2 bHLH Domain−DNA Complex:  Heterodimer Selectivity and DNA Recognition ,
journal, January 2008

  • Longo, Antonella; Guanga, Gerald P.; Rose, Robert B.
  • Biochemistry, Vol. 47, Issue 1
  • DOI: 10.1021/bi701527r

Base-resolution maps of 5-formylcytosine and 5-carboxylcytosine reveal genome-wide DNA demethylation dynamics
journal, January 2015

  • Lu, Xingyu; Han, Dali; Zhao, Boxuan Simen
  • Cell Research, Vol. 25, Issue 3
  • DOI: 10.1038/cr.2015.5

Single-base resolution analysis of active DNA demethylation using methylase-assisted bisulfite sequencing
journal, November 2014

  • Wu, Hao; Wu, Xiaoji; Shen, Li
  • Nature Biotechnology, Vol. 32, Issue 12
  • DOI: 10.1038/nbt.3073

5-formylcytosine and 5-carboxylcytosine reduce the rate and substrate specificity of RNA polymerase II transcription
journal, July 2012

  • Kellinger, Matthew W.; Song, Chun-Xiao; Chong, Jenny
  • Nature Structural & Molecular Biology, Vol. 19, Issue 8
  • DOI: 10.1038/nsmb.2346

Building a schizophrenia genetic network: transcription factor 4 regulates genes involved in neuronal development and schizophrenia risk
journal, June 2018

  • Xia, Hanzhang; Jahr, Fay M.; Kim, Nak-Kyeong
  • Human Molecular Genetics, Vol. 27, Issue 18
  • DOI: 10.1093/hmg/ddy222

Coot model-building tools for molecular graphics
journal, November 2004

  • Emsley, Paul; Cowtan, Kevin
  • Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
  • DOI: 10.1107/S0907444904019158

Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010


Single-Base Resolution Analysis of 5-Formyl and 5-Carboxyl Cytosine Reveals Promoter DNA Methylation Dynamics
journal, February 2015


Using a structural and logics systems approach to infer bHLH–DNA binding specificity determinants
journal, February 2011

  • De Masi, Federico; Grove, Christian A.; Vedenko, Anastasia
  • Nucleic Acids Research, Vol. 39, Issue 11
  • DOI: 10.1093/nar/gkr070

Quantitative Analysis of the DNA Methylation Sensitivity of Transcription Factor Complexes
journal, June 2017


PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
  • DOI: 10.1107/S0907444909052925

5-Hydroxymethylcytosine in E-box motifs ACAT|GTG and ACAC|GTG increases DNA-binding of the B-HLH transcription factor TCF4
journal, January 2016

  • Khund-Sayeed, Syed; He, Ximiao; Holzberg, Timothy
  • Integrative Biology, Vol. 8, Issue 9
  • DOI: 10.1039/C6IB00079G

Medulloblastoma and ependymoma cells display increased levels of 5-carboxylcytosine and elevated TET1 expression
journal, February 2017


Genomic distribution of 5‐formylcytosine and 5‐carboxylcytosine in human preimplantation embryos
journal, November 2018

  • Pendina, Anna A.; Efimova, Olga A.; Krapivin, Mikhail I.
  • Molecular Reproduction and Development, Vol. 85, Issue 12
  • DOI: 10.1002/mrd.23074

Impact of cytosine methylation on DNA binding specificities of human transcription factors
journal, May 2017


Carbon-Oxygen Hydrogen Bonding in Biological Structure and Function
journal, October 2012

  • Horowitz, Scott; Trievel, Raymond C.
  • Journal of Biological Chemistry, Vol. 287, Issue 50
  • DOI: 10.1074/jbc.R112.418574

Cognitive and Sensorimotor Gating Impairments in Transgenic Mice Overexpressing the Schizophrenia Susceptibility Gene Tcf4 in the Brain
journal, July 2010


Measurement of protein by spectrophotometry at 205 nm
journal, May 1974


Structure and function of helix-loop-helix proteins
journal, June 1994

  • Murre, Cornelis; Bain, Gretchen; van Dijk, Marc A.
  • Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1218, Issue 2
  • DOI: 10.1016/0167-4781(94)90001-9

A Sensitive Approach to Map Genome-wide 5-Hydroxymethylcytosine and 5-Formylcytosine at Single-Base Resolution
journal, February 2015


TRIM8-driven transcriptomic profile of neural stem cells identified glioma-related nodal genes and pathways
journal, February 2019

  • Venuto, Santina; Castellana, Stefano; Monti, Maria
  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1863, Issue 2
  • DOI: 10.1016/j.bbagen.2018.12.001

A survey of rare coding variants in candidate genes in schizophrenia by deep sequencing
journal, October 2013


Multiparametric scaling of diffraction intensities
journal, April 2003

  • Otwinowski, Zbyszek; Borek, Dominika; Majewski, Wladyslaw
  • Acta Crystallographica Section A Foundations of Crystallography, Vol. 59, Issue 3
  • DOI: 10.1107/S0108767303005488

Sequence-specific recognition of double helical nucleic acids by proteins.
journal, March 1976

  • Seeman, N. C.; Rosenberg, J. M.; Rich, A.
  • Proceedings of the National Academy of Sciences, Vol. 73, Issue 3
  • DOI: 10.1073/pnas.73.3.804

Phaser crystallographic software
journal, July 2007

  • McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
  • Journal of Applied Crystallography, Vol. 40, Issue 4
  • DOI: 10.1107/S0021889807021206

Two distinct transcription factors that bind the immunoglobulin enhancer microE5/kappa 2 motif
journal, January 1990


Tcf4 regulates dendritic spine density and morphology in the adult brain
journal, June 2018


Tet3 Reads 5-Carboxylcytosine through Its CXXC Domain and Is a Potential Guardian against Neurodegeneration
journal, January 2016


Haploinsufficiency of TCF4 Causes Syndromal Mental Retardation with Intermittent Hyperventilation (Pitt-Hopkins Syndrome)
journal, May 2007

  • Zweier, Christiane; Peippo, Maarit M.; Hoyer, Juliane
  • The American Journal of Human Genetics, Vol. 80, Issue 5
  • DOI: 10.1086/515583